OF PARASITES OF WILD EUROPEAN RABBITS ORYCTOLAGUS CUNICULUS (L.)

Transcription

1 J. Parasitl., 85(5), 1999 p ? merican Sciety f Parasitlgists 1999 FCTORS INFLUNCING TH FCL GG ND OOCYST COUNTS OF PRSITS OF WILD UROPN RBBITS ORYCTOLGUS CUNICULUS (L.) IN SOUTHRN WSTRN USTRLI Russell P. Hbbs, Laurie Twigg*, ileen D. llit, and manda G. Wheeler* Divisin f Veterinary and Bimedical Sciences, Murdch University, Murdch W 615, ustralia BSTRCT: bundance f intestinal parasites was mnitred by fecal egg and cyst cunts fr samples f wild rabbits Oryctlagus cuniculus with different levels f impsed female sterility frm 12 ppulatins in suthwestern ustralia. Differences in egg cunts f Trichstrngylus retrtaefrmis between seasns and age grups were dependent n the sex f the hst. Pregnancy may have been respnsible fr these differences because egg cunts were cnsistently higher in intact females than in females surgically sterilized by tubal ligatin. gg cunts fr Passalurus ambiguus were influenced by seasn and hst age but there were n differences between sexes r between intact and sterilized female rabbits. N differences were detected in the cyst cunts f the 8 species f imeria between male and female rabbits r between intact and sterilized females. Seasnal differences were detected in cyst cunts f imeria flavescens and imeria stiedai. The verwhelming determinant f cccidian cyst cunts was hst age, with 6 species being much mre abundant in rabbits up t 4 m f age. There was a suggestin that egg cunts f T. retrtaefrmis and cyst cunts f several species f imeria were reduced in ppulatins where rabbit numbers had been depressed fr at least 2 yr, but there was n evidence that shrt-term variatins in rabbit numbers had a measurable effect n parasite abundance. Nematde and cccidian parasitism f wild urpean rabbits (Oryctlagus cuniculus (L.)) is influenced by hst age and sex. In ustralia, the influence f age is particularly imprtant fr species f imeria (Mykytwycz, 1962). Hst age, sex and reprductive status all affect parasitism with Trichstrngylus retrtaefrmis, and pregnancy is a risk factr (Dunsmre and Dudzinski, 1968). field study set up t determine the effects next mrning and split int 2 subsamples: ne placed in 1% frmalin f impsing 4 levels f female sterility (%, 4%, 6%, 8%) and the ther in 2.5% ptassium dichrmate. Samples were nt chsen n rabbit ppulatins in suthwestern ustralia (Twigg et al., randmly as they were dependent n defecatin by trapped rabbits. 1998) prvided an pprtunity t investigate further the effectswhere pssible, we cllected samples frm 1 kittens and subadults f hst age and sex, pregnancy, and seasn n parasitism by cccidia and nematdes. The 12 discrete free-ranging ppulatins varied cnsiderably in rabbit numbers particularly because sme f the higher sterility regimes were successful in reducing ppulatin size (Hbbs et al., 1999). This variatin enabled us t investigate the relatinship between hst ppulatin size and parasite abundance. lthugh there has been a great deal f attentin given t theretical aspects f the ppulatin dynamics f infectius disease since the intrductin f the mathematical mdels f ndersn and May (1979), there have been calls fr mre empirical studies n the dynamics f these diseases, particularly with respect t the density-dependent relatinships between hst and parasite (e.g., Dbsn and Hudsn, 1995; McCallum, 1995). MTRILS ND MTHODS The rabbit sterility trials were lcated in the wheat belt regin f suthwestern Western ustralia near Wellstead (34?3'S 118?36'). Cli- and placed n a micrscpe slide. The entire cverslip was scanned at mate is Mediterranean, with lng dry summers during which time there is little breeding by rabbits. The annual average rainfall is 5 mm, cncentrated in the cler mnths f May t Nvember, althugh sme summer rainfall is nrmal (Twigg et al., 1998). Twelve discrete ppulatins f rabbits were established t determine the level f female sterility that is required t cause a sustained reductin in rabbit abundance. ll sites were situated n the brder f narrw strips f native vegetatin refuges and annual pastures. ach site was fenced in a flat- Received 4 March 1998; revised 23 February 1999; accepted 23 February * Vertebrate Pest Research Services, griculture Western ustralia, and Vertebrate Bicntrl CRC, Bugainvillea venue, Frrestfield, W 658, ustralia. tened U shape such that breeding stps were cnfined t a strip f native vegetatin m X 6-1 m, while allwing access t adjacent pasture n the pen side fr fd. Female rabbits were surgically sterilized by tubal ligatin in the prprtin f %, 4%, 6%, and 8%, with 3 replicates f each treatment. Sham peratins were included such that 8% f females received sme frm f surgery. Live-capture cage traps were set vernight (Twigg et al., 1996). Fresh fecal samples were cllected frm the grund under ccupied traps the (< 1,2 g bdy mass) and 1 adults at each f 6 sampling perids fr each rabbit ppulatin. ttal f 1,297 samples was cllected, frm Octber 1994 t March 1996, with the mst intensive sampling during late winter and spring f Fr 1,77 f these samples, the birth date f each rabbit culd be back-calculated frm the bdy mass at time f first capture, prvided that the bdy mass was < 1, g at that time. The calculatin was based n a birth mass f 5 g and a grwth rate f 1 g per day (Twigg et al., 1998). Fr seasn and sex cmparisns, age categries were based n bdy mass f rabbits at the time f sampling; kittens (<7 g), subadults (7-1,199 g), and adults (>1,199 g), whereas fr hst abundance cmparisns, yung rabbits were thse < 1, g. We cunted nematde eggs by a fltatin technique. n aliqut f 14 ml f water was added t apprximately 1 ml f frmalin-fixed feces in a graduated centrifuge tube that was spun fr 3 sec at 5 g. We determined the vlume f the fecal plug t the nearest.1 ml. The plug was washed thrughly with water thrugh a.8-mm mesh sieve, then centrifuged at 5 g fr 2 min. The supernatant was discarded and the plug resuspended in sufficient saturated NaNO3 t frm a psitive meniscus. cverslip edged with Vaseline was placed ver the tp f the centrifuge tube and left t stand fr 15 min, and then carefully remved 1X magnificatin, and all eggs were cunted. We recrded the number f eggs per ml f feces as eggs per g (epg) fr simplicity. Cccidian cysts were cunted n a single pass thrugh the middle f the cverslip at 4X magnificatin. If there were <5 cysts cunted n that pass, a secnd pass was made clse t the first. s the cverslip was 4 field-widths wide at that magnificatin, the number f cysts per ml feces was estimated as: number f cysts/ml = (4 X number cunted)/[number f passes X vlume f feces (ml)]. The number f cysts/ml was recrded as cysts/g. Repeatability f the cyst cunting technique was established by variance cmpnents accrding t the methd f Yvre et al. (1992). We ran 1 scans n each f 2 cverslip preparatins f 6 fecal samples and determined that repeatability was.95 fr scans f the same cverslip preparatin and.92 fr preparatins f the same sample. Strngyle eggs were differentiated by their 796

2 HOBBS T L.-PRSIT POPULTIONS IN WILD RBBITS 797 Q ) 5, 2- c) ,) 9t- a) 5- I'... Kitten Juvenile Y1 Y2 Y3 FIGUR 1. Gemetric means f egg cunts f Trichstrngylus retrtaefrmis in males, intact females, sham-perated females, and sterilized females. ge grups are kittens (up t 66 days), juveniles ( days), Y1 ( days), Y2 ( days), and Y3 (73 r mre days ld). Sterilizatins were undertaken (January-March) after rabbit recruitment had ccurred each year. Sample sizes are shwn abve each pint length. ggs f Graphidium strigsum are larger than thse f T. retrtaefrmis (Bull, 1953). The ther parasite eggs present in the fecal samples were easily identified as the xyurid nematde Passalurus ambiguus, which ccurs in the large intestine and cecum. We used the ptassium dichrmate subsamples t separate the species f imeria by identifying 5 sprulated cysts fr each psitive sample (Hbbs and Twigg, 1998). Fr sme samples with very lw cunts (1% f the ttal), we were unable t find 5 cysts, and species differentiatin was based n fewer cysts. The effects f sex, sterility status, seasn (cllecting perid), and age n parasite egg and cyst cunts were determined by Mann-Whitney r Kruskal-Wallis nnparametric tests using Statview 4. (bacus Cncepts, Berkeley, Califrnia). The effect f hst abundance n parasite egg and cyst cunts was tested by linear regressin analysis f the gemetric means (i.e., back-calculated means f lg-transfrmed data) f parasite egg cunts and the minimum number f rabbits knwn t be alive (MNK) apprximately 1 m prir t fecal cllectin fr thse cllectin grups where there were at least 1 fecal samples. ach f 2 age grups based n bdy mass at time f capture were tested separately. Mann-Whitney tests were used t cmpare egg and cyst cunt f the 3 lwest-density rabbit ppulatins with thse f the ther 9 ppulatins and als the 3 highest-density ppulatins with the ther 9. RSULTS Only 2 species f nematde parasite, T. retrtaefrmis and P. ambiguus, were detected in ur rabbits. Pstmrtem examinatin f the intestines f 14 rabbits at the end f the sterility study cnfirmed the presence f these species. Ocysts f 1 species f imeria were detected, and their prevalences have been reprted in Hbbs and Twigg (1998), but nly the 8 mst prevalent f these species are discussed here. Lg-lg scatter plts f T. retrtaefrmis egg cunts against hst age indicated that there was n bvius decline in parasitism with age (data nt shwn). Hwever, almst all the rabbits lder than 1 yr with high cunts f T. retrtaefrmis were intact r sham-perated females. Thus, the data were split by sex and sterility status fr further analysis. Figure 1 shws gemetric means fr thse rabbits fr which the date f birth was knwn. The highest cunts were in juveniles, and there was a decline in cunts as rabbits became adult. There were further declines in subsequent year classes in male rabbits and sterilized females but nt in intact r sham-perated females. Cunts in juveniles were significantly higher than in kittens r adults (Table I). mng adults during breeding perids, cunts were significantly higher in intact female rabbits than in males and lwer in sterilized females than sham-perated females (Table I). gg cunts f T. retrtaefrmis were significantly higher during breeding perids than during nnbreeding perids fr intact and sham-perated females (Table II). Hwever there was n such difference fr sterilized females, and the difference fr males was very small (Table II). There were n differences between sexes fr any f the age grups fr cunts f P. ambiguus during breeding perids (Table I). gg cunts were significantly higher in adult rabbits, but prevalence was t lw t test fr the presence f a decline in rabbits lder than 1 yr ld. There was n difference in cunts between intact and sterilized female rabbits (Table I). gg cunts were higher during nnbreeding perids in adult rabbits (Table III). Fr the cccidia, there were highly significant differences in cyst cunts recrded frm rabbits f different ages fr all 8 species but n differences between sexes fr any age grup (Table I). Gemetric mean cyst cunts and prevalences fr thse rabbits f knwn age are given in Figures 2 and 3, respectively. Fr all cccidian species except imeria pirifrmis and imeria flavescens, the highest cyst cunts were frm either kitten r juvenile rabbits. Ocyst cunts were higher in adult rabbits fr bth pirifrmis and flavescens. There were seasnal differences in abundance in nly 2 species f imeria. Breeding perid cyst cunts were higher in imeria stiedai, whereas nnbreeding perid cunts were higher in flavescens (Table III). Details f linear regressins f gemetric mean egg and cyst cunts against hst ppulatin size (MNK) measured apprximately 1 m prir t fecal cllectin are shwn in Table IV. We expected psitive slpes, but nne were significant at P -.1. Similar results were btained using ther measures f rabbit ppulatin size, and when ppulatins were measured at the time f fecal cllectin r 4 m prir. Only 2 regressins apprached significance, including that f T. retrtaefrmis in yung rabbits, but it was apparent frm the scatterplt (Fig. 4) that variatin was high. Figure 5 shws the scatterplt fr imeria magna where a psitive slpe apprached significance fr adult rabbits. Hwever, a single utlier pint at high rabbit ppulatin size was respnsible fr the effect, and althugh that cyst cunt was high fr adult rabbits, it was lwer than mst means fr yunger rabbits. Thus, ur regressin analyses shw that the abundance f rabbits had little effect n parasite egg and cyst cunts at the rabbit densities we encuntered. Hwever, prevalences f all species were generally quite high s it is likely that all ur rabbit densities were high enugh t ensure adequate transmissin. We therefre cmpared egg and cyst cunts fr the 3 sites with lwest rabbit densities t thse f the ther sites (Table V). The 3 lw-density sites included 2 frm the 8% sterility grup and 1 frm the 6% grup, and althugh there were strng fluctuatins in ppulatin size, these ppulatins were cnsistently in the lwest third except fr a single cllecting perid when 1 ppulatin was measured as fifth highest. There were n significant differences in parasitism

3 -. TBL I. Sample sizes, gemetric means, and statistical significance fr effects f hst age* and sex n fecal egg and cyst cunts during the breeding dults Kittens Juveniles Sham- Steri P P Intact perated ize Males Females (sex)t Males Females (sex)t Males females P (sex)t females female Sample sizes (nematdes) Trichstrngylus retrtaefrmis < Passalurus ambiguus Sample sizes (cccidia) I imeria exigua perfrans intestinalis pirifrmis media flavescens magna stiedai * ge grups are based n bdy mass at time f capture: kittens (<7 g), juveniles (7-1,199 g), adults (>1,199 g). t Significance (Mann-Whitney) between males and intact females within age grup. : Significance (Mann-Whitney) between sham-perated and sterilized adult females.? Significance (Kruskal-Wallis) between age grups (sexes cmbined). Fr adults, nly males and intact females are included. 1 Sample sizes are smaller fr cccidia because many samples did nt sprulate s that species culd nt be differentiated.?[ ls tested separately within sex: males (P <.1), intact females (P <.1) i-.- * cr ld C OC p > D 3 C 4D a pi. 1.''.'" N~~~~ nr3 &a' q ks) ( -J U)ON O en <O? u ChC O c U4>>< ^-.'lu) ( ( P (S a n)so OC ^ n) 7L^ > )? CN(tQ I 2 a ve ac. &' V! Cs * I? S. 5. ^5 S- ~. Cs c l1?q=. m 3 Q m O P: a ' 3 O3 r C? _ C:5 a N 3. Is 3 4^ C- S^'- z r N Cs C >. _ sc 2 rd a nc)) 3?.? BO. Cs_ D B ^If? : r O C 5 (D S. (=-. x C- D _ O' C Cs * as (5 -t Cs B 3r Cs O s -t eb 8 CsQ (^ ( dbs ^ a CsC- Cs 3,^ Cs B " - i. a t Cs T. G-" 11 I? Cs1a - C z C) CsCJQ B.a C B ; C) Cs *. i - z Q Cs >. 5 :. I.I 51! w< p y, 3. C). g S Da.a? 5. P. B? 5. a Y ( Cs B-in B 5 x - I ^ - a a a - C<. a Cs ^S,?, " C/3? CQ3 a a ' a' t z m _ Cy V CT Ha (D l a x 3 ON ^ ('D ri l tn t5 U) F D D ^ <I y? ' ( ( ( 2i. c2, ~ 5 5 < Lr, - N s (8 (,-- ~j~-( w -- :, J9, (- (= - U) C-' (- -j L?J -41?~ -

4 - HOBBS T L.-PRSIT POPULTIONS IN WILD RBBITS 799 ) 3( 6( c C a)._2 4C D 2C Kitten Juvenile Y 1 Y2 Y 3 ge grup FIGUR 2. Gemetric means f cyst cunts f species f imeria in rabbits f different age. ge grups are kittens (up t 66 days), juveniles ( days), Y1 ( days), Y2 ( days), and Y3 (73 r mre days ld). t an actual decline in wrm numbers r an effect n fecundity f the wrms. Dunsmre (1966a) and Dunsmre and Dudzinski in which estrgen implants resulted in increased burdens f naturally acquired T retrtaefrmis in bth males and females (Dunsmre, 1971). There has been much interest in the effect f reprductive hrmnes n immunity t nematde parasitism in dmestic ruminants. lthugh prlactin levels have been assciated with a periparturient rise in egg cunts, it is nw becming clear that prlactin is nt the cause f this phenmenn (Jeffcate et al., 199; Barger, 1993). In ur study the sterilized females had lwer egg cunts. These rabbits were already adult when sterilized, and bth varies and Fallpian tubes remained intact because the methd f sterilizatin was tubal ligatin. They als ften underwent pseudpregnancy, and in cntrast t Dunsmre's (1966a) rabbits, they wuld have been hrmnally intact. Thus, ur results cnflict with Dunsmre's (1966a) high wrm burdens in thse rabbits that had their Fallpian tubes remved, but it shuld be pinted ut that his sample size was nly 1 rabbits per grup. The differences that we fund between sterilized and entire female rabbits appear t be due t factrs assciated with pregnancy ther than reprductive hrmnes. Further study is needed t cnfirm these findings. The abundance f P. ambiguus was seasnal and age related but did nt appear t be affected by hst sex. gg cunts were highest in the late summer samples when there were n kittens. In Wales (U.K.), where the breeding seasn is in late spring, P. ambiguus were fund t have higher prevalences and intensities in winter, utside the breeding seasn (vans, 194). This was attributed t a greater prprtin f yung, uninfected rabbits in the breeding seasn samples. Hwever, this was nt a factr (1968) reprted a difference in wrm cunts between sexes, particularly late in the breeding seasn. Dunsmre (1966a) reprted that female rabbits that had been sterilized by the remval f their Fallpian tubes and that underwent pseudpregnancies had T. retrtaefrmis burdens almst as high as intact cluded frm the analysis. It is als surprising that the highest in ur study because kittens and juveniles <1, g were ex- females. Females sterilized by variectmy, hwever, harbred egg cunts ccurred in summer in ur study, because the area much lwer wrm burdens, similar t thse in males. Dunsmre is subject t quite ht and relatively dry summers. There was (1966a) cncluded that reprductive hrmnes were respnsible abve average rain prir t the March 1996 sample (Twigg et fr these differences, and this was supprted by a later study al., 1998), but the cunt was similar t the March 1995 sample 1 --O --a exigua perfrans intestinalis 8- pirifrmis media fla vescens U)6 magna stiedai CO n4- Kitten Juvenile Y1 Y2 Y3 ge grup FIGUR 3. Prevalence (%) f species f imeria in rabbits f different age. ge grups are kittens (up t 66 days), juveniles ( days), Y1 ( days), Y2 ( days), and Y3 (73 r mre days ld).

5 8 TH JOURNL OF PRSITOLOGY, VOL. 85, NO. 5, OCTOBR 1999 TBL IV. nalysis f variance fr regressin f gemetric means f egg and cyst cunts against hst abundance.* Yung rabbitst dult rabbits n Slpe F P n Slpe F P Trichstrngylus retrtaefrmis t Passalurus ambiguus 19? imeria exigua perfrans intestinalis pirifrmis media flavescens magna stiedai * Gemetric means are based n grups f cllectin peri t Yung rabbits are thse with bdy mass <1, g. t Samples frm March each year (summer nnbreeding perid) were excluded because egg cunts were lw.? Samples ther than March each year were excluded because egg cunts were lw. that fllwed average rain. Dunsmre (1966b) fund P. ambiguus t be relatively rare at his mst arid site. The prepatent perid fr this species is abut 2 m, and the delay befre egg prductin may be the cause f the shift f the peak frm early t late summer. ls, it is likely that the eggs f P. ambiguus are relatively resistant t desiccatin. In summer, rabbits are eating clser t the grund and therefre cme int clser cntact with the infective eggs. This is in cntrast t T. retrtaefrmis fr which the infective stage is a mtile larva that can climb ff the grund and nt fd plants. The effect f hst age n the abundance f cccidia is well recgnized (Bull, 1958; Mykytwycz, 1962) and has been shwn t be due t hst immunity rather than physilgy ndersn, (Stdart, 1968a). lthugh the prevalence f pirifrmis cntinulatins may underg higher stress resulting in lwer immunity 1979). In additin, individuals in higher density ppued t increase with hst age in ur study, cyst cunts that culd enhance establishment and reprductin f parasites reached a peak at abut 1 yr f age. This suggests that hst (Llyd, 1995). Our study has demnstrated the difficulty f detecting the effect f hst density n parasitism in the wild. We immunity acts t limit an existing infectin rather than by preventing a new infectin at least in this species. We were unable expected density-dependent effects t shw up clearly in the t find seasnal patterns in cccidian cyst cunts except fr regressin analyses, yet nne were detected. One explanatin is that ur fecal egg and cyst cunts might nt have related t real parasite abundance. Hwever, we have shwn that presn <?n I I I a I I uv Breeding seasn, yung.. ^ Breeding seasn, adults x Nn-breeding seasn, adults Yung c) a) CL 4- flavescens and stiedai. This may be explained partly by the lack f seasnality in rainfall patterns during ur study perid due t lwer winter rainfall and unusually high rainfall in December 1995 (Twigg et al., 1998). Cccidian cysts n pasture require mild temperatures and a relatively mist envirnment fr sprulatin and survival. Stdart (1968b) fund peaks in abundance after gd rains at her semiarid sites and cnsidered rainfall t be a majr factr determining seasnality. The abundance f parasites that utilize the ral rute f infectin and that have direct life cycles is assumed t increase in higher density hst ppulatins by increased transmissin rate due t increased cntact frequency between hsts (May and c c? 2 - x dults C) a) U 3- C. c) ) 15- >, -1 ^ ' ' X. x Ox-- -- x x ---X--~...x... X X _.,, K X x. c c 1- c CU 5- Q) 2i'. x x x xx x Y~,l_,i,,' x... x Rabbit ppulatin size (MNK) Rabbit ppulatin FIGUR 4. Regressin f gemetric mean egg cunts l gylus retrtaefrmis at different cllectin sites, against r tin size measured apprximately 1 m prir t fecal cll rabbits are thse with bdy mass < 1, g. FIGUR 5. Regressin f gemetric mean egg cunts f imeria magna at different cllectin sites, against rabbit ppulatin size measured apprximately 1 m prir t fecal cllectin. Yung rabbits are thse with bdy mass <1, g.

6 HOBBS T L.-PRSIT POPULTIONS IN WILD RBBITS 81 TBL V. Nnparametric Mann-Whitney significance levels (P) fr cmparisns between sites f different rabbit density. Lw density vs. thers * High density vs. therst Yungt: dults Cmbined Yung dults Cmbined Trichstrngylus retrtaefrmis ?.95.3? Passalurus ambiguus imeria exigua ?.68? perfrans ? intestinalis pirifrmis ? media ? fiavescens magna ? stiedai * The lw-density grup cntains rabbits frm the 3 s ther 9 sites. t The high-density grup cntains rabbits frm the 3 sites with the highest rabbit densities ver the perid f the study. These rabbits are cmpared t rabb the ther 9 sites. t Yung rabbits are thse with bdy mass <1, g.? Significant and expected effect (P <.1) where the rabbits frm higher density sites have higher egg r cyst cunts. Significant but unexpected effect (P <.1) where the rabbits frm lwer density sites have higher egg r cyst cunts. viusly knwn patterns f nematde ppulatin distributins in rabbits accrding t seasn, hst age, and sex were detectable using fecal egg cunts, s we can be reasnably cnfident that ur egg cunts d reflect wrm numbers. In ther intensively Bilgical Cntrl f Vertebrate Pest Ppulatins, and was cn- studied hsts, egg cunts d crrelate with wrm burdens (e.g., ducted under nimal thics apprval frm griculture Western Cabaret et al., 1998). Cccidian cyst cunts may nt reflect ustralia (91L58). abundance f the rganisms in an individual, but the mean cunt frm a ppulatin f rabbits shuld reflect the abundance and transmissin rate in that ppulatin (Yvre and snault, 1987). secnd explanatin fr the lack f significant regressins is that there were in fact n density-dependent relatinships. Hwever, ur cntrasts between sites with lng-term lwdensity rabbit ppulatins and the ther sites did prvide sme evidence fr density dependence. Thus, it appears that the shrtterm fluctuatins in bth hst and parasite abundance may have bscured the lng-term trend. New Zealand study where rabbit numbers underwent a gradual decline ver a perid f 5 yr shwed that the abundance f the nematdes T. retrtaefrmis and G. strigsum, and 2 spp. f imeria als declined (Bull, 1957). It is interesting that althugh we detected declines at lw densities fr several parasite species, we detected nly 1 case f enhancement at higli densities. This suggests that cntact with infective stages is nrmally high, and nly at lw hst densities is it lw enugh t result in lwer abundance. s a crllary t this, if the density-dependent effect is due t stress (Llyd, 1995), then we must cnclude that at Wellstead, stress is the nrmal state. Parasites are thught t cntribute t the regulatin f natural ppulatins f their hsts by reducing their fecundity and survival. If this is density dependent, then there must be a relatinship between hst density and parasitism, irrespective f the mechanism f the regulatry effect (Hlmes, 1995). t the hst densities and parasite abundances bserved in ur study, evidence fr such a relatinship was equivcal. CKNOWLDGMNTS We thank ur numerus clleagues fr their assistance with varius aspects f this study, particularly the cllectin f fecal pellets. We als thank Jn Dunsmre, Ian Rbertsn, and ndrew Thmpsn fr their very helpful cmments n the manuscript. This study was funded by the griculture Prtectin Bard, W (griculture Western ustralia) and the CRC fr LITRTUR CITD NDRSON, R. M., ND R. M. MY Ppulatin bilgy f infectius diseases. Part I. Nature 28: BRGR, I Influence f sex and reprductive status n susceptibility f ruminants t nematde parasitism. Internatinal Jurnal fr Parasitlgy 23: BULL, P. C Parasites f the wild rabbit, Oryctlagus cuniculus (L.) in New Zealand. New Zealand Jurnal f Science and Technlgy B 34: Changing incidence f parasites in a declining rabbit ppulatin. Prceedings f the New Zealand clgical Sciety 5: Incidence f cccidia (Sprza) in wild rabbits, Oryctlagus cuniculus (L.), in Hawke's Bay, New Zealand. New Zealand Jurnal f Science 1: CBRT, J., N. GSNIR, ND P. JCQUIT Faecal egg cunts are representative f digestive tract strngyle wrm burdens in sheep and gats. Parasite 5: DOBSON,. P., ND P. J. HUDSON Micrparasites: Observed patterns in wild animal ppulatins. In clgy f infectius diseases in natural ppulatins, B. T Grenfell and. P. Dbsn (eds.). Cambridge University Press, Cambridge, U.K., p DUNSMOR, J. D. 1966a. Influence f hst reprductin n numbers f trichstrngylid nematdes in the urpean rabbit, Oryctlagus cuniculus (L.). Jurnal f Parasitlgy 52: b. Nematde parasites f free-living rabbits, Oryctlagus cuniculus (L.), in eastern ustralia III. Variatins in the number f Passalurus ambiguus (Rudlphi) Railliet & Henry. ustralian Jurnal f Zlgy 14: Influence f hst hrmnes n nematde parasitism in rabbits, Oryctlagus cuniculus (L.). ustralian Jurnal f Zlgy 19: , ND M. L. DUDZINSKI Relatinship f numbers f nematde parasites in wild rabbits, Oryctlagus cuniculus (L.), t hst sex, age, and seasn. Jurnal f Parasitlgy 54: VNS, W. M. R Observatins n the incidence f sme nematde parasites f the cmmn rabbit, Oryctlagus cuniculus. Parasitlgy 32:

7 82 TH JOURNL OF PRSITOLOGY, VOL. 85, NO. 5, OCTOBR 1999 HOBBS, R. P., ND L. TWIGG Cccidia (imeria spp.) f wild rabbits in suthwestern ustralia. ustralian Veterinary Jurnal 76: ,. D. LLIOT, ND. G. WHLR valuatin f an assciatin f parasitism with mrtality f wild urpean rabbits Oryctlagus cuniculus (L.) in suthwestern ustralia. Jurnal f Parasitlgy 85: HOLMS, J. C Ppulatin regulatin: dynamic cmplex f interactins. Wildlife Research 22: JFFCOT, I.., G. FISHWICK, K. BIRDN, J. RMOUR, ND P. H. HOL- MS Pathphysilgy f the periparturient egg rise in sheep: The rle f prlactin. Research in Veterinary Science 48: LLOYD, S nvirnmental influences n hst immunity. In clgy f infectius diseases in natural ppulatins, B. T. Grenfell and. P. Dbsn (eds.). Cambridge University Press, Cambridge, U.K., p MY, R. M., ND R. M. NDRSON Ppulatin bilgy f infectius diseases: Part II. Nature 28: MCCLLUM, H. I Mdelling wildlife-parasite interactins t help plan and interpret field studies. Wildlife Research 22: MYKYTOWYCZ, R pidemilgy f cccidisis (imeria spp.) in an experimental ppulatin f the ustralian wild rabbit, Oryctlagus cuniculus (L.). Parasitlgy 52: STODRT, 1968a. Cccidisis in wild rabbits, Oryctlagus cuniculus (L.), at fur sites in different climatic regins in eastern ustralia. I. Relatinship with the age f the rabbit. ustralian Jurnal f Zlgy 16: b. Cccidisis in wild rabbits, Oryctlagus cuniculus (L.), at fur sites in different climatic regins in eastern ustralia. II. The relatinship f cyst utput t climate and sme aspects f the rabbit's physilgy. ustralian Jurnal f Zlgy 16: TWIGG, L., S. L. GRIFFIN, ND C. M. O'RILLY Live capture techniques fr the urpean rabbit. Western ustralian Naturalist 21: , T. J. LOW, G. R. MRTIN,. G. WHLR, G. S. GRY, S. L. GRIFFIN, C. M. O'RILLY, T. L. BUTLR, D. J. ROBINSON, ND P. H. HUBCH The eclgy f the urpean rabbit (Oryctlagus cuniculus) in castal suthern Western ustralia. Wildlife Research 25: YVOR, P., J. CBRT, ND S. SOLON Repeatability f vine faecal cyst cunts in natural infectins with imeria spp. Internatinal Jurnal fr Parasitlgy 22: , ND. SNULT Interpreting fecal examinatins fr vine and caprine cccidial infectin. Veterinary Medicine 82: